A Ralstonia solanacearum type III effector alters the actin and microtubule cytoskeleton to promote bacterial virulence in plants

PLoS Pathog. 2024 Dec 26;20(12):e1012814. doi: 10.1371/journal.ppat.1012814. eCollection 2024 Dec.

Abstract

Cellular responses to biotic stress frequently involve signaling pathways that are conserved across eukaryotes. These pathways include the cytoskeleton, a proteinaceous network that senses external cues at the cell surface and signals to interior cellular components. During biotic stress, dynamic cytoskeletal rearrangements serve as a platform from which early immune-associated processes are organized and activated. Bacterial pathogens of plants and animals use proteins called type III effectors (T3Es) to interfere with host immune signaling, thereby promoting virulence. We previously found that RipU, a T3E from the soilborne phytobacterial pathogen Ralstonia solanacearum, co-localizes with the plant cytoskeleton. Here, we show that RipU from R. solanacearum K60 (RipUK60) associated with and altered the organization of both the actin and microtubule cytoskeleton. We found that pharmacological disruption of the tomato (Solanum lycopersicum) cytoskeleton promoted R. solanacearum K60 colonization. Importantly, tomato plants inoculated with R. solanacearum K60 lacking RipUK60 (ΔripUK60) had reduced wilting symptoms and significantly reduced root colonization when compared to plants inoculated with wild-type R. solanacearum K60. Collectively, our data suggest that R. solanacearum K60 uses the type III effector RipUK60 to remodel cytoskeletal organization, thereby promoting pathogen virulence.

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism
  • Bacterial Proteins* / metabolism
  • Cytoskeleton / metabolism
  • Microtubules* / metabolism
  • Plant Diseases* / microbiology
  • Ralstonia solanacearum* / metabolism
  • Ralstonia solanacearum* / pathogenicity
  • Solanum lycopersicum* / microbiology
  • Type III Secretion Systems / metabolism
  • Virulence

Substances

  • Bacterial Proteins
  • Type III Secretion Systems
  • Actins

Grants and funding

This work was funded by a Foundation for Food and Agriculture (FFAR) New Innovator Award to AIP and the EMBRIO Institute, contract #2120200, a National Science Foundation (NSF) Biology Integration Institute (CS and AIP). We are also grateful for support from the Ohio State University Presidential Student and Postdoctoral Fellowships to TLK and MVM, respectively. This research was also funded, in part, by the United States Department of Agriculture, Agricultural Research Service (USDA-ARS) research project 5020-21220-014-00D. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. All opinions expressed in this paper are the authors’ and do not necessarily reflect the policies and views of USDA. USDA is an equal opportunity provider and employer. USDA-ARS provided salary for MH and NJ.